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Marine Biology

, 165:110 | Cite as

Green sea turtle (Chelonia mydas) population history indicates important demographic changes near the mid-Pleistocene transition

  • Robert R. FitakEmail author
  • Sönke Johnsen
SHORT NOTES

Abstract

The increased availability of genome sequences has provided remarkable advances in our understanding of the evolutionary history of non-model species. One important consideration in evolutionary studies is the role of demographic history in shaping contemporary levels and distribution of genetic variation. In green sea turtles (Chelonia mydas), a draft genome sequence has recently been made available, yet little is known regarding how past demographic events have shaped genomic variation in populations of this species. In this study, single nucleotide polymorphisms were identified in the green sea turtle’s genome and used to reconstruct past demographic events. It was found that this green sea turtle population, from the South China Sea, experienced a marked expansion ca. 0.8 million years ago near the mid-Pleistocene transition (MPT). Simulations revealed that the past demographic history can at least partially be explained by changes in population structure and gene flow; possibly associated with the climatic and geomagnetic events occurring since the MPT. The results demonstrate the importance in considering the effects of gene flow when reconstructing historical changes in population size and provide an extensive set of genomic resources for future evolutionary studies of green sea turtles.

Notes

Acknowledgements

We thank the Duke Shared Cluster Resource for providing the computational resources, and A. Ochoa and K. Lohmann for comments on earlier drafts of this manuscript. We also appreciate the comments and suggestions from the reviewers for improving the manuscript. This study was supported by a grant from the Air Force Office of Scientific Research (#FA9550-14-1-0208) to SJ.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The article does not contain any experiments with animals performed by any of the authors.

Data availability

All sequence data are available within the NCBI BioProject database (accession no. PRJNA104937), polymorphism data and simulation results are available in Pangaea (https://doi.pangaea.de/10.1594/PANGAEA.890759), and analysis code and computer scripts are available in GitHub (https://github.com/rfitak/GST_Demographic_History).

References

  1. Akey JM, Eberle MA, Rieder MJ, Carlson CS, Shriver MD, Nickerson DA, Kruglyak L (2004) Population history and natural selection shape patterns of genetic variation in 132 genes. PLoS Biol 2:e286.  https://doi.org/10.1371/journal.pbio.0020286 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5:181–190.  https://doi.org/10.1002/zoo.1430050212 CrossRefGoogle Scholar
  3. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709.  https://doi.org/10.1038/nrg2844 CrossRefPubMedGoogle Scholar
  4. Amemiya CT, Alfoldi J, Lee AP et al (2013) The African coelacanth genome provides insights into tetrapod evolution. Nature 496:311–316.  https://doi.org/10.1038/nature12027 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bickham JW, Bjorndal KA, Haiduk MW, Rainey WE (1980) The karyotype and chromosomal banding patterns of the green turtle (Chelonia mydas). Copeia 1980:540–543.  https://doi.org/10.2307/1444535 CrossRefGoogle Scholar
  6. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120.  https://doi.org/10.1093/bioinformatics/btu170 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Cande SC, Kent DV (1995) Revised calibration of the geomagnetic polarity timescale for the late Cretaceous and Cenozoic. J Geophys Res 100:6093–6095.  https://doi.org/10.1029/94jb03098 CrossRefGoogle Scholar
  8. Chan CX, Ragan MA (2013) Next-generation phylogenomics. Biol Direct 8:3.  https://doi.org/10.1186/1745-6150-8-3 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Clement BM (2004) Dependence of the duration of geomagnetic polarity reversals on site latitude. Nature 428:637–640.  https://doi.org/10.1038/nature02459 CrossRefPubMedGoogle Scholar
  10. Danecek P, Auton A, Abecasis G et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158.  https://doi.org/10.1093/bioinformatics/btr330 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Denton JF, Lugo-Martinez J, Tucker AE, Schrider DR, Warren WC, Hahn MW (2014) Extensive error in the number of genes inferred from draft genome assemblies. PLoS Comput Biol 10:e1003998.  https://doi.org/10.1371/journal.pcbi.1003998 CrossRefPubMedPubMedCentralGoogle Scholar
  12. DePristo MA, Banks E, Poplin R et al (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43:491–498.  https://doi.org/10.1038/ng.806 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dethmers KE, Broderick D, Moritz C et al (2006) The genetic structure of Australasian green turtles (Chelonia mydas): exploring the geographical scale of genetic exchange. Mol Ecol 15:3931–3946.  https://doi.org/10.1111/j.1365-294X.2006.03070.x CrossRefPubMedGoogle Scholar
  14. Dutton PH, Jensen MP, Frey A et al (2014) Population structure and phylogeography reveal pathways of colonization by a migratory marine reptile (Chelonia mydas) in the central and eastern Pacific. Ecol Evol 4:4317–4331.  https://doi.org/10.1002/ece3.1269 PubMedPubMedCentralCrossRefGoogle Scholar
  15. Elderfield H, Ferretti P, Greaves M, Crowhurst S, McCave IN, Hodell D, Piotrowski AM (2012) Evolution of ocean temperature and ice volume through the mid-Pleistocene climate transition. Science 337:704–709.  https://doi.org/10.1126/science.1221294 CrossRefPubMedGoogle Scholar
  16. Ellegren H (2014) Genome sequencing and population genomics in non-model organisms. Trends Ecol Evol 29:51–63.  https://doi.org/10.1016/j.tree.2013.09.008 CrossRefPubMedGoogle Scholar
  17. Endres DM, Schindelin JE (2003) A new metric for probability distributions. IEEE Trans Inf Theory 49:1858–1860.  https://doi.org/10.1109/TIT.2003.813506 CrossRefGoogle Scholar
  18. Fitak RR, Mohandesan E, Corander J, Burger PA (2016) The de novo genome assembly and annotation of a female domestic dromedary of North African origin. Mol Ecol Resour 16:314–324.  https://doi.org/10.1111/1755-0998.12443 CrossRefPubMedGoogle Scholar
  19. Glassmeier KH, Vogt J (2010) Magnetic polarity transitions and biospheric effects. Space Sci Rev 155:387–410.  https://doi.org/10.1007/s11214-010-9659-6 CrossRefGoogle Scholar
  20. Green RE, Braun EL, Armstrong J et al (2014) Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science 346:1254449.  https://doi.org/10.1126/science.1254449 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Head MJ, Pillans B, Farquhar SA (2008) The early-middle Pleistocene transition: characterization and proposed guide for the defining boundary. Episodes 31:255–259Google Scholar
  22. Hellenthal G, Stephens M (2007) msHOT: modifying Hudson’s ms simulator to incorporate crossover and gene conversion hotspots. Bioinformatics 23:520–521.  https://doi.org/10.1093/bioinformatics/btl622 CrossRefPubMedGoogle Scholar
  23. Hudson RR (2002) Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18:337–338.  https://doi.org/10.1093/bioinformatics/18.2.337 CrossRefPubMedGoogle Scholar
  24. Hwang S, Kim E, Lee I, Marcotte EM (2015) Systematic comparison of variant calling pipelines using gold standard personal exome variants. Sci Rep 5:17875.  https://doi.org/10.1038/srep17875 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Jensen MP, FitzSimmons NN, Dutton PH (2013) Molecular genetics of sea turtles. In: Wyneken J, Lohmann KJ, Musick JA (eds) Biology of sea turtles, vol III. CRC Press, Boca Raton, pp 135–161CrossRefGoogle Scholar
  26. Jensen MP, Pilcher N, FitzSimmons NN (2016) Genetic markers provide insight on origins of immature green turtles Chelonia mydas with biased sex ratios at foraging grounds in Sabah, Malaysia. Endanger Species Res 31:191–201.  https://doi.org/10.3354/esr00763 CrossRefGoogle Scholar
  27. Joseph J, Nishizawa H, Arshaad WM et al (2016) Genetic stock compositions and natal origin of green turtle (Chelonia mydas) foraging at Brunei Bay. Glob Ecol Conserv 6:16–24.  https://doi.org/10.1016/j.gecco.2016.01.003 CrossRefGoogle Scholar
  28. Kitaba I, Hyodo M, Katoh S, Dettman DL, Sato H (2013) Midlatitude cooling caused by geomagnetic field minimum during polarity reversal. Proc Natl Acad Sci U S A 110:1215–1220.  https://doi.org/10.1073/pnas.1213389110 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kolinski SP, Cruce J, Parker DM, Balazs GH, Clarke R (2014) Migrations and conservation implications of post-nesting green turtles from Gielop Island, Ulithi Atoll, Federated States of Micronesia. Micronesica 2014–04:1–9Google Scholar
  30. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760.  https://doi.org/10.1093/bioinformatics/btp324 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Li H, Durbin R (2011) Inference of human population history from individual whole-genome sequences. Nature 475:493–496.  https://doi.org/10.1038/nature10231 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Li H, Handsaker B, Wysoker A et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079.  https://doi.org/10.1093/bioinformatics/btp352 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lohmann KJ, Lohmann CM, Ehrhart LM, Bagley DA, Swing T (2004) Animal behaviour: geomagnetic map used in sea-turtle navigation. Nature 428:909–910.  https://doi.org/10.1038/428909a CrossRefPubMedGoogle Scholar
  34. Luschi P, Benhamou S, Girard C, Ciccione S, Roos D, Sudre J, Benvenuti S (2007) Marine turtles use geomagnetic cues during open-sea homing. Curr Biol 17:126–133.  https://doi.org/10.1016/j.cub.2006.11.062 CrossRefPubMedGoogle Scholar
  35. Mazet O, Rodriguez W, Grusea S, Boitard S, Chikhi L (2016) On the importance of being structured: instantaneous coalescence rates and human evolution-lessons for ancestral population size inference? Heredity 116:362–371.  https://doi.org/10.1038/hdy.2015.104 CrossRefPubMedGoogle Scholar
  36. McMahon BJ, Teeling EC, Hoglund J (2014) How and why should we implement genomics into conservation? Evol Appl 7:999–1007.  https://doi.org/10.1111/eva.12193 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Nadachowska-Brzyska K, Burri R, Smeds L, Ellegren H (2016) PSMC analysis of effective population sizes in molecular ecology and its application to black-and-white Ficedula flycatchers. Mol Ecol 25:1058–1072.  https://doi.org/10.1111/mec.13540 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Ng CKY, Dutton PH, Gu HX et al (2017) Regional conservation implications of green turtle (Chelonia mydas) genetic stock composition in China. Chelonian Conserv Biol 16:139–150.  https://doi.org/10.2744/CCB-1253.1 CrossRefGoogle Scholar
  39. Nishizawa H, Okuyama J, Kobayashi M, Abe O, Arai N (2010) Comparative phylogeny and historical perspectives on population genetics of the Pacific hawksbill (Eretmochelys imbricata) and green turtles (Chelonia mydas), inferred from feeding populations in the Yaeyama Islands, Japan. Zoolog Sci 27:14–18.  https://doi.org/10.2108/zsj.27.14 CrossRefPubMedGoogle Scholar
  40. Nishizawa H, Narazaki T, Fukuoka T, Sato K, Hamabata T, Kinoshita M, Arai N (2014) Juvenile green turtles on the northern edge of their range: mtDNA evidence of long-distance westward dispersals in the northern Pacific Ocean. Endanger Species Res 24:171–179CrossRefGoogle Scholar
  41. Pool JE, Hellmann I, Jensen JD, Nielsen R (2010) Population genetic inference from genomic sequence variation. Genome Res 20:291–300.  https://doi.org/10.1101/gr.079509.108 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Read TC, Wantiez L, Werry JM, Farman R, Petro G, Limpus CJ (2014) Migrations of green turtles (Chelonia mydas) between nesting and foraging grounds across the Coral Sea. PLoS ONE 9:e100083.  https://doi.org/10.1371/journal.pone.0100083 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Reece JS, Castoe TA, Parkinson CL (2005) Historical perspectives on population genetics and conservation of three marine turtle species. Conserv Genet 6:235–251.  https://doi.org/10.1007/s10592-004-7821-y CrossRefGoogle Scholar
  44. Roden SE, Morin PA, Frey A, Balazs GH, Zarate P, Cheng IJ, Dutton PH (2013) Green turtle population structure in the Pacific: new insights from single nucleotide polymorphisms and microsatellites. Endanger Species Res 20:227–234.  https://doi.org/10.3354/esr00500 CrossRefGoogle Scholar
  45. Seminoff JA (2004) Chelonia mydas. The IUCN Red List of Threatened Species.  https://doi.org/10.2305/IUCN.UK.2004.RLTS.T4615A11037468.en (Accessed 25 June 2017) CrossRefGoogle Scholar
  46. Senko J, López-Castro MC, Koch V, Nichols WJ (2010) Immature East Pacific green turtles (Chelonia mydas) use multiple foraging areas off the Pacific coast of Baja California Sur, Mexico: first evidence from mark-recapture data. Pac Sci 64:125–130.  https://doi.org/10.2984/64.1.125 CrossRefGoogle Scholar
  47. Shaffer HB, Minx P, Warren DE et al (2013) The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage. Genome Biol 14:R28.  https://doi.org/10.1186/gb-2013-14-3-r28 CrossRefPubMedGoogle Scholar
  48. van de Wal RSW, de Boer B, Lourens LJ, Köhler P, Bintanja R (2011) Reconstruction of a continuous high-resolution CO2 record over the past 20 million years. Clim Past 7:1459–1469.  https://doi.org/10.5194/cp-7-1459-2011 CrossRefGoogle Scholar
  49. Wang Z, Pascual-Anaya J, Zadissa A et al (2013) The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan. Nat Genet 45:701–706.  https://doi.org/10.1038/ng.2615 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276CrossRefPubMedGoogle Scholar
  51. Yang W, Wang Y, Chen M (2015) Genetic structure and diversity of green sea turtle (Chelonia mydas) from South China Sea inferred by mtDNA control region sequence. Biochem Syst Ecol 60:95–98.  https://doi.org/10.1016/j.bse.2015.04.007 CrossRefGoogle Scholar
  52. Zhao H, Qiang X, Sun Y (2014) Apparent timing and duration of the Matuyama–Brunhes geomagnetic reversal in Chinese loess. Geochem Geophys Geosyst 15:4468–4480.  https://doi.org/10.1002/2014GC005497 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyDuke UniversityDurhamUSA

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